Meprin A impairs epithelial barrier function, enhances monocyte migration, and cleaves the tight junction protein occludin

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 5, 2013, Pages

  Bao, Jialing ^a   Yura, Renee E ^a   Matters, Gail L ^a   Bradley, S Gaylen ^a   Shi, Pan ^a   Tian, Fang ^a   Bond, Judith S ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Knockout mice; Madin Darby canine kidney cells; Metalloproteinase; Tight junction proteins

Indexed keywords

CLAUDIN 4; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; FLUORESCEIN SODIUM; MEPRIN; MEPRIN B; METALLOPROTEINASE; OCCLUDIN; RECOMBINANT PROTEIN; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING ORGAN SYSTEMS; BLADDER PERMEABILITY; CELL MIGRATION; CONTROLLED STUDY; ENZYME INHIBITION; EPITHELIAL BARRIER FUNCTION; EXTRACELLULAR MATRIX; HUMAN; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; KIDNEY EPITHELIUM; MDCK CELL; MONOCYTE; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; RAT; WILD TYPE;

EID: 84883436572     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00179.2012     Document Type: Article

References (53)

1. Al-Sadi R, Khatib K, Guo S, Ye D, Youssef M, Ma T. Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 300: G1054-G1064, 2011.
2. Ando-Akatsuka Y, Saitou M, Hirase T, Kishi M, Sakakibara A, Itoh M, Yonemura S, Furuse M, Tsukita S. Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J Cell Biol 133: 43-47, 1996.
3. Awad AS, Kinsey GR, Khutsishvili K, Gao T, Bolton WK, Okusa MD. Monocyte/macrophage chemokine receptor CCR2 mediates diabetic renal injury. Am J Physiol Renal Physiol 301: F1358-F1366, 2011.
4. Bamforth SD, Kniesel U, Wolburg H, Engelhardt B, Risau W. A dominant mutant of occludin disrupts tight junction structure and function. J Cell Sci 112: 1879-1888, 1999.
5. Banerjee S, Oneda B, Yap LM, Jewell DP, Matters GL, Fitzpatrick LR, Seibold F, Sterchi EE, Ahmad T, Lottaz D, Bond JS. MEP1A allele for meprin A metalloprotease is a susceptibility gene for inflammatory bowel disease. Mucosal Immunol 2: 220-231, 2009.
6. Bertenshaw GP, Norcum MT, Bond JS. Structure of homo- and heterooligomeric meprin metalloproteases. Dimers, tetramers, and high molecular mass multimers. J Biol Chem 278: 2522-2532, 2003.
7. Bertenshaw GP, Turk BE, Hubbard SJ, Matters GL, Bylander JE, Crisman JM, Cantley LC, Bond JS. Marked differences between metalloproteases meprin A and B in substrate and peptide bond specificity. J Biol Chem 276: 13248-13255, 2001.
8. Bertenshaw GP, Villa JP, Hengst JA, Bond JS. Probing the active sites and mechanisms of rat metalloproteases meprin A and B. Biol Chem 383: 1175-1183, 2002.
9. Bond JS, Matters GL, Banerjee S, Dusheck RE. Meprin metalloprotease expression and regulation in kidney, intestine, urinary tract infections and cancer. FEBS Lett 579: 3317-3322, 2005.
10. Bylander J, Li Q, Ramesh G, Zhang B, Reeves WB, Bond JS. Targeted disruption of the meprin metalloproteinase beta gene protects against renal ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol 294: F480-F490, 2008.
11. Bylander JE, Bertenshaw GP, Matters GL, Hubbard SJ, Bond JS. Human and mouse homo-oligomeric meprin A metalloendopeptidase: substrate and inhibitor specificities. Biol Chem 388: 1163-1172, 2007.
12. Chung NP, Mruk D, Mo MY, Lee WM, Cheng CY. A 22-amino acid synthetic peptide corresponding to the second extracellular loop of rat occludin perturbs the blood-testis barrier and disrupts spermatogenesis reversibly in vivo. Biol Reprod 65: 1340-1351, 2001.
13. Crisman JM, Zhang B, Norman LP, Bond JS. Deletion of the mouse meprin beta metalloprotease gene diminishes the ability of leukocytes to disseminate through extracellular matrix. J Immunol 172: 4510-4519, 2004.
14. Cummins PM. Occludin: one protein, many forms. Mol Cell Biol 32: 242-250, 2012.
15. D'Souza T, Agarwal R, Morin PJ. Phosphorylation of claudin-3 at threonine 192 by cAMP-dependent protein kinase regulates tight junction barrier function in ovarian cancer cells. J Biol Chem 280: 26233-26240, 2005.
16. Dunay IR, Damatta RA, Fux B, Presti R, Greco S, Colonna M, Sibley LD. Gr1_ inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29: 306-317, 2008.
17. Edens HA, Parkos CA. Modulation of epithelial and endothelial paracellular permeability by leukocytes. Adv Drug Deliv Rev 41: 315-328, 2000.
18. Eichel L, Scheidweiler K, Kost J, Shojaie J, Schwarz E, Messing E, Wood R. Assessment of murine bladder permeability with fluorescein: validation with cyclophosphamide and protamine. Urology 58: 113-118, 2001.
19. Elias BC, Suzuki T, Seth A, Giorgianni F, Kale G, Shen L, Turner JR, Naren A, Desiderio DM, Rao R. Phosphorylation of Tyr-398 and Tyr-402 in occludin prevents its interaction with ZO-1 and destabilizes its assembly at the tight junctions. J Biol Chem 284: 1559-1569, 2009.
20. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123: 1777-1788, 1993.
21. Grant-Tschudy KS, Wira CR. Hepatocyte growth factor regulation of uterine epithelial cell transepithelial resistance and tumor necrosis factor alpha release in culture. Biol Reprod 72: 814-821, 2005.
22. Harhaj NS, Felinski EA, Wolpert EB, Sundstrom JM, Gardner TW, Antonetti DA. VEGF activation of protein kinase C stimulates occludin phosphorylation and contributes to endothelial permeability. Invest Ophthalmol Vis Sci 47: 5106-5115, 2006.
23. Hirase T, Staddon JM, Saitou M, Ando-Akatsuka Y, Itoh M, Furuse M, Fujimoto K, Tsukita S, Rubin LL. Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 110: 1603-1613, 1997.
24. Huber D, Balda MS, Matter K. Occludin modulates transepithelial migration of neutrophils. J Biol Chem 275: 5773-5778, 2000.
25. Huguenin M, Muller EJ, Trachsel-Rosmann S, Oneda B, Ambort D, Sterchi EE, Lottaz D. The metalloprotease meprinbeta processes Ecadherin and weakens intercellular adhesion. PLos One 3: e2153, 2008.
26. Huppert J, Closhen D, Croxford A, White R, Kulig P, Pietrowski E, Bechmann I, Becher B, Luhmann HJ, Waisman A, Kuhlmann CR. Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J 24: 1023-1034, 2010.
27. Kaushal GP, Haun RS, Herzog C, Shah SV. Meprin A metalloproteinase and its role in acute kidney injury. Am J Physiol Renal Physiol 304: F1150-F1158, 2013.
28. Lacaz-Vieira F, Jaeger MM, Farshori P, Kachar B. Small synthetic peptides homologous to segments of the first external loop of occludin impair tight junction resealing. J Membr Biol 168: 289-297, 1999.
29. Li L, Huang L, Sung SS, Vergis AL, Rosin DL, Rose CE. Jr, Lobo PI, Okusa MD. The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury. Kidney Int 74: 1526-1537, 2008.
30. Matters GL, Manni A, Bond JS. Inhibitors of polyamine biosynthesis decrease the expression of the metalloproteases meprin α and MMP-7 in hormone-independent human breast cancer cells. Clin Exp Metastasis 22: 331-339, 2005.
31. Medina R, Rahner C, Mitic LL, Anderson JM, Van Itallie CM. Occludin localization at the tight junction requires the second extracellular loop. J Membr Biol 178: 235-247, 2000.
32. Muller SL, Portwich M, Schmidt A, Utepbergenov DI, Huber O, Blasig IE, Krause G. The tight junction protein occludin and the adherens junction protein _-catenin share a common interaction mechanism with ZO-1. J Biol Chem 280: 3747-3756, 2005.
33. Norman LP, Jiang W, Han X, Saunders TL, Bond JS. Targeted disruption of the meprin _ gene in mice leads to underrepresentation of knockout mice and changes in renal gene expression profiles. Mol Cell Biol 23: 1221-1230, 2003.
34. Ongeri EM, Anyanwu O, Reeves WB, Bond JS. Villin and actin in the mouse kidney brush-border membrane bind to and are degraded by meprins, an interaction that contributes to injury in ischemia-reperfusion. Am J Physiol Renal Physiol 301: F871-F882, 2011.
35. Ostermann G, Weber KS, Zernecke A, Schroder A, Weber C. JAM-1 is a ligand of the _2 integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol 3: 151-158, 2002.
36. Phillips BE, Cancel L, Tarbell JM, Antonetti DA. Occludin independently regulates permeability under hydrostatic pressure and cell division in retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 49: 2568-2576, 2008.
37. Raleigh DR, Marchiando AM, Zhang Y, Shen L, Sasaki H, Wang Y, Long M, Turner JR. Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell 21: 1200-1213, 2010.
38. Red Eagle AR, Hanson RL, Jiang W, Han X, Matters GL, Imperatore G, Knowler WC, Bond JS. Meprin beta metalloprotease gene polymorphisms associated with diabetic nephropathy in the Pima Indians. Hum Genet 118: 12-22, 2005.
39. Reibman J, Hsu Y, Chen LC, Bleck B, Gordon T. Airway epithelial cells release MIP-3α/CCL20 in response to cytokines and ambient particulate matter. Am J Respir Cell Mol Biol 28: 648-654, 2003.
40. Reyes JL, Lamas M, Martin D, del Carmen Namorado M, Islas S, Luna J, Tauc M, Gonzalez-Mariscal L. The renal segmental distribution of claudins changes with development. Kidney Int 62: 476-487, 2002.
41. Roche WR, Montefort S, Baker J, Holgate ST. Cell adhesion molecules and the bronchial epithelium. Am Rev Respir Dis 148: S79-82, 1993.
42. Runkle EA, Sundstrom JM, Runkle KB, Liu X, Antonetti DA. Occludin localizes to centrosomes and modifies mitotic entry. J Biol Chem 286: 30847-30858, 2011.
43. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11: 4131-4142, 2000.
44. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR. Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73: 283-309, 2011.
45. Sonoda N, Furuse M, Sasaki H, Yonemura S, Katahira J, Horiguchi Y, Tsukita S. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: evidence for direct involvement of claudins in tight junction barrier. J Cell Biol 147: 195-204, 1999.
46. Sterchi EE, Stocker W, Bond JS. Meprins, membrane-bound and secreted astacin metalloproteinases. Mol Aspects Med 29: 309-328, 2008.
47. Sun Q, Jin HJ, Bond JS. Disruption of the meprin α and β genes in mice alters homeostasis of monocytes and natural killer cells. Exp Hematol 37: 346-356, 2009.
48. Van Itallie CM, Fanning AS, Anderson JM. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins. Am J Physiol Renal Physiol 285: F1078-F1084, 2003.
49. Wachtel M, Frei K, Ehler E, Fontana A, Winterhalter K, Gloor SM. Occludin proteolysis and increased permeability in endothelial cells through tyrosine phosphatase inhibition. J Cell Sci 112: 4347-4356, 1999.
50. Wang X, Gill RL. Jr, Zhu Q, Tian F. Bacterial expression, purification, and model membrane reconstitution of the transmembrane and cytoplasmic domains of the human APP binding protein LR11/SorLA for NMR studies. Protein Expr Purif 77: 224-230, 2011.
51. Wang Z, Mandell KJ, Parkos CA, Mrsny RJ, Nusrat A. The second loop of occludin is required for suppression of Raf1-induced tumor growth. Oncogene 24: 4412-4420, 2005.
52. Wilcox RA, Wada DA, Ziesmer SC, Elsawa SF, Comfere NI, Dietz AB, Novak AJ, Witzig TE, Feldman AL, Pittelkow MR, Ansell SM. Monocytes promote tumor cell survival in T-cell lymphoproliferative disorders and are impaired in their ability to differentiate into mature dendritic cells. Blood 114: 2936-2944, 2009.
53. Yura RE, Bradley SG, Ramesh G, Reeves WB, Bond JS. Meprin A metalloproteases enhance renal damage and bladder inflammation after LPS challenge. Am J Physiol Renal Physiol 296: F135-F144, 2009.